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European Journal of Radiology
journal homepage: www.elsevier.com/locate/ejrad
Assesment of perfusion in glial tumors with arterial spin labeling;
comparison with dynamic susceptibility contrast method
H Cebeci a,∗ , O Aydin a , E Ozturk-Isik b , C Gumus b , F Inecikli c , A Bekar d ,
H Kocaeli d , B Hakyemez a
a
Department of Radiology, Uludag University Medical School, Bursa, Turkey
Department of Biomedical Engineering, Yeditepe University, Istanbul, Turkey
c
Department of Radiology, Kanuni Sultan Suleyman Educational and Research Hospital, Istanbul, Turkey
d
Department of Neurosurgery, Uludag University Medical School, Bursa, Turkey
b
a r t i c l e
i n f o
Article history:
Received 8 November 2013
Received in revised form 30 June 2014
Accepted 7 July 2014
Keywords:
Glioma
Dynamic susceptibility contrast perfusion
imaging
Arterial spin labeling
a b s t r a c t
Purpose: Arterial spin labeling perfusion imaging (ASL-PI) is a non-invasive perfusion imaging method
that can be used for evaluation and quantification of cerebral blood flow (CBF). Aim of our study was
to evaluating the efficiency of ASL in histopathological grade estimation of glial tumors and comparing
findings with dynamic susceptibility contrast perfusion imaging (DSC-PI) method.
Methods: This study involved 33 patients (20 high-grade and 13 low-grade gliomas). Multiphase multislice
pulsed ASL MRI sequence and a first-passage gadopentetate dimeglumine T2*-weighted gradient-echo
single-shot echo-planar sequence were acquired for all the patients. For each patient, perfusion relative
signal intensity (rSI), CBF and relative CBF (rCBF) on ASL-PI and relative cerebral blood volume (rCBV) and
relative cerebral blood flow (rCBF) values on DSC-PI were determined. The relative signal intensity of each
tumor was determined as the maximal SI within the tumor divided by SI within symetric region in the
contralateral hemisphere on ASL-PI. rCBV and rCBF were calculated by deconvolution of an arterial input
function. Relative values of the lesions were obtained by dividing the values to the normal appearing
symmetric region on the contralateral hemisphere. For statistical analysis, Mann–Whitney ranksum test
was carried out. Receiver operating characteristic curve (ROC) analysis was performed to assess the
relationship between the rCBF-ASL, rSI-ASL, rCBV and rCBF ratios and grade of gliomas. Their cut-off
values permitting best discrimination was calculated. The correlation between rCBV, rCBF, rSI-ASL and
rCBF-ASL and glioma grade was assessed using Spearman correlation analysis.
Results: There was a statistically significant difference between low and high-grade tumors for all parameters. Correlation analyses revealed significant positive correlations between rCBV and rCBF-ASL (r = 0.81,
p < 0.001). However correlation between rCBF and rCBF-ASL was weaker (r = 0.64, p < 0.001).
Conclusion: Arterial spin labeling is an employable imaging technique for evaluating tumor perfusion
non-invasively and may be useful in differentiating high and low grade gliomas.
© 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction
Brain tumors constitute one of the important disease group and
frequently difficulties are encountered in imaging [1]. Glial tumors
are the most common primary neoplasms of the brain in adults, and
histopathological distribution of gliomas were complex between
low grade and high grade [2]. Histopathological grading of brain
tumors which is achieved by surgical excision or stereotactic biopsy
is crucial for optimal treatment planning [3].
∗ Corresponding author. Tel.: +90 224 2953341.
E-mail address: [email protected] (H. Cebeci).
Magnetic resonance (MR) imaging in particular is the most
frequently used imaging modality to evaluate brain tumors.
In addition to conventional MR sequences, advanced MR techniques found their place in clinical practice. Perfusion imaging,
diffusion-weighted imaging, and MR spectroscopic imaging are the
commonly used advanced MR imaging methods for brain tumor
evaluation. These advanced techniques generate physiological data
and information on chemical composition [1].
In general, contrast-enhanced conventional cranial MR imaging is mostly sufficient for intracranial tumor diagnosis. But there
are some limitations, like nonspecificity of contrast enhancement.
Enhancement after contrast agent reflects blood brain barrier
disruption rather than a true assessment of tumor vascularity.
http://dx.doi.org/10.1016/j.ejrad.2014.07.002
0720-048X/© 2014 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: Cebeci H, et al. Assesment of perfusion in glial tumors with arterial spin labeling; comparison with
dynamic susceptibility contrast method. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.07.002
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H. Cebeci et al. / European Journal of Radiology xxx (2014) xxx–xxx
Especially, differential diagnosis between high and low-grade
tumors and between radiation necrosis and recurrent tumors are
challenges by using only conventional contrast-enhanced cranial
MRI [4,5].
Recent advances in dynamic MR imaging have enabled the
assessment of tumor vascularity quantitatively. Among various
functional imaging techniques, perfusion MR imaging is particularly sensitive in demonstrating microvasculature and tumor
neovascularization. Clinical applications of perfusion MR imaging
in brain tumor evaluation include assessment of tumoral grade,
achieving guidance for stereotactic biopsy, differentiation between
recurrent glioma and radiation necrosis, and determination of prognosis and response to treatment [4,5].
Perfusion MR imaging methods exploit signal changes that
accompany the passage of tracer through the cerebrovascular system. The tracer can be endogenous (arterial water) or exogenous
(deuterium oxide, gadopentetate dimeglumine). Arterial spin labeling (ASL) MRI is a perfusion imaging method, which uses arterial
blood water as a freely diffusible endogenous tracer [6]. One of the
exogenous tracer methods of perfusion imaging is dynamic susceptibility contrast perfusion imaging (DSC-PI). In DSC-PI, rapid loss of
MR signal on T2* weighted images is measured and then used to
calculate the change in concentration of contrast material for each
individual voxel [7].
The goal of our study was to determine the usefulness of ASL in
evaluating the histopathological grade of cerebral gliomas and to
compare findings with DSC-PI method.
2. Materials and methods
2.1. Patient population
This retrospective study included thirty-three patients with
histopathologically proven gliomas (18 male, 15 female; age
range = 17 to 74 years, mean age = 46.9 years) who had undergone perfusion MRI examination in our institute with both ASL
and DSC perfusion imaging methods between January 2010 and
May 2013. In total, we investigated twenty high-grade and thirteen
low-grade gliomas. Histopathological diagnosis was obtained with
surgical excision for all tumors. The grading of gliomas was based
on 2007 World Health Organization brain tumor classification [8].
The study was approved by institutional ethical committee. The
lesions were eighteen glioblastome multiforme, one grade 3 astrocytoma, one gliosarcoma, eleven grade 2 oligodendroglioma, one
disembryoblastic neuroepithelial tumor (DNET), and one pilocytic
astrocytoma.
2.2. Imaging protocol
All MR imaging examinations were performed on a clinical 3
Tesla MR imaging system (Philips Achieva 3T, Best, Netherlands)
by using a 32 channel head coil. For conventional MR study, axial
3D turbo field echo (TFE) (TR/TE = 8.1/3.7 ms), axial T2-weighted
turbo spin-echo (TSE) (TR/TE = 3000/80 ms), and axial post-contrast
3D-TFE images were acquired.
Multiphase ASL method was used in all patients. ASL-PI studies were performed after conventional MR sequences. ASL was
capable of multisection image acquisition at multiple inversion
time points (multiple TI) and was based on the EPISTAR pulsed
ASL technique. On the basis of conventional MR imaging results,
we selected 6 transverse sections through the tumor for our
ASL studies. Image acquisition was done at 8 TI times. For the
first slice, minimum inversion time was 300 ms, and subsequent
inversion times were increased by 250 ms. The labeling slab thickness was 130 mm, and it was positioned at the level of upper
cervical region. The imaging parameters for the ASL sequence were
as follows: TR/TE = 250/16 ms, flip angle = 40◦ , FOV = 240 × 240 cm,
matrix = 68 × 68, slice thickness/gap = 6/0.6 mm, number of dynamics = 30. A total of 2880 images, including 1440 labeled and 1440
control images, were obtained. The total acquisition time was 4 min
and 8 s. ASL images were transferred to an off-line workstation
(Philips Extended MR workspace, R.2.6.3.2, 2009) and subtraction
images and rCBF maps were obtained.
DSC-PI was performed after ASL image acquisition by a first
passage contrast-enhanced T2-weighted single-shot gradient-echo
echo-planar sequence. The parameters of the sequence were as
follows: TR/TE = 1513/40 ms, flip angle = 75◦ , FOV = 224 × 224 mm,
matrix = 96 × 95, slice thickness = 5 mm, slice gap = 0 mm, and total
data acquisition time = 65 s. As a contrast material, 20 ml gadodiamide (Omniscan, Nycomed, Norway) was administered using an
18 ga IV catheter at a rate of 5 ml/s automatically (Spectris Solaris EP
MR Injection System, Medrad) by the antecubital venous method.
This was followed by 20 ml serum physiological liquid injection at
nearly the same rate. After the perfusion MRI, contrast-enhanced
T1-weighted 3D-TFE sequence was acquired.
2.3. Data processing
Image analysis was performed in Extended MR workspace
(Version 2.6.3.2, 2009, Philips Medical Systems) with the special
application tools “neuro perfusion” and “image algebra” for DSCPI and ASL-PI, respectively. After evaluating the conventional MRI
sequences, ASL and DSC images were evaluated and perfusion
maps are created. Qualitative interpretation of lesions on perfusion
images did not performed.
In ASL data processing, 48 subtraction images of the labeled and
control images were obtained. A manually drawn elliptic region
of interest (ROI) was placed on the solid and brightest portion of
tumor seen in subtraction images, which was assumed as having
high perfusion. The signal intensity of the lesion was normalized
with the symmetrical region on the contralateral normal hemisphere (rSI). A program was written in MATLAB (The Mathworks
Inc., Natick, MA) for calculating the absolute cerebral blood flow
from ASL images. First, thirty dynamics of each slice were averaged to increase SNR. Brain tissue was masked from the control
images for each slice. Main magnetization (M0) was estimated for
each pixel of the masked images using the T1 relaxation equation at different phases of control images using T1 value of blood
(1.664 s). Thereafter, cerebral blood flow was calculated by taking
into account the arterial blood flow [9]. The inversion efficiency (˛)
was used as 0.95, T1 of tissue was used as 1.3 s, and the blood tissue
water partition coefficient was taken as 0.9 for the whole brain.
For DSC data processing, arterial input function model was used.
Middle cerebral artery (MCA) was selected as an arterial input for
assessing CBF and CBV maps. For obtaining normalized values, the
symmetrical region on the contralateral hemisphere was accepted
as reference like in ASL data processing.
2.4. Statistical analysis
Five perfusion MRI parameters, which were rCBV and rCBF
obtained from DSC-PI and CBF, rCBF, and rSI values obtained from
ASL were evaluated. The capability of these perfusion values and
ratios about differentiating low and high-grade gliomas was investigated with Mann-Whitney ranksum test. Bonferroni multiple
comparison correction was used, and a p value of less than 0.01
was considered as significant. The correlation between perfusion
parameters obtained with DSC and ASL was assessed using Spearman correlation analysis.
Receiver operating characteristic curve analysis was used to
evaluate the association between the perfusion values and the
Please cite this article in press as: Cebeci H, et al. Assesment of perfusion in glial tumors with arterial spin labeling; comparison with
dynamic susceptibility contrast method. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.07.002
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Fig. 1. A 53 years old woman diagnosed with oligodendroglioma grade 2. Conventional T2W (A), T1W (B) and postcontrast T1W (C) MR images, show a large, nonenhancing
mass in the left frontal lobe. CBV (D) and CBF (E) maps of DSC-PI and ASL subtraction image (F) show hypoperfusion in tumoral lesion.
grade of the glioma, as well as to calculate cutoff values permitting
discrimination between high and low-grade gliomas.
3. Results
On conventional MRI findings, twenty-two out of thirty-three
lesions had contrast enhancement. Nineteen of the enhancing
lesions were high-grade, and 3 of them were low grade gliomas.
All the perfusion parameters obtained with ASL and DSC-PI were
successful in the discrimination of low and high-grade gliomas
(p < 0.001, using the Mann–Whitney rank sum test). There were
significant differences between low and high-grade gliomas for all
the parameters. The mean values of the parameters assessed in low
and high-grade gliomas, and p values of the Mann–Whitney rank
Table 1
The age and sex distributions and perfusion parameters of low and high-grade
gliomas.
Sex (%male)
Age
rCBV
rCBF
rCBF ASL
rSI ASL
CBF ASL
Low grade (n = 13)
High grade (n = 20)
p
69.2
41.5 ± 15
0.89 (0.43–4.08)
0.85 (0.36–3.62)
0.96 (0.22–2.14)
0.93 (0.54–2.29)
8.1 (4.6–117)
45
51.3 ± 15.6
4.15 (2–7.14)
2.55 (1.54–5.8)
4.7 (2.44–7.95)
4.87 (2.21–21.32)
23.65 (6.8–186)
0.17
0.1
<0.001
<0.001
<0.001
<0.001
<0.001
rCBV, relative cerebral blood volume; rCBF, relative cerebral blood flow; rCBF ASL,
relative cerebral blood flow obtained with ASL; rSI ASL, relative signal intensity
obtained with ASL; CBF ASL, cerebral blood flow obtained with ASL.
sum test are shown in Table 1. Figs. 1 and 2 show example cases of
a low-grade and a high-grade glioma, respectively.
For ASL perfusion imaging parameters, a cut-off value of 2.10
and 2.19 for ASL-rCBF and ASL-rSI ratios, respectively (sensitivity %100, specifity %92.3), were the values for best discrimination.
Fig. 3 shows the ROC curves for the perfusion parameters assessed
in this study. As a result of the correlation analyses between perfusion parameters, a strong correlation between rCBV and ASL-rCBF
(r = 0.81, p < 0.001) was found. However, the correlation between
rCBF and ASL-rCBF was weaker (r = 0.64, p < 0.001). There was also
a strong correlation between rCBV and ASL-rSI (r = 0.83, p < 0.001),
ASL-rCBF and ASL-rSI (r = 0.76, p < 0.001), and ASL-rCBF and ASL-CBF
(r = 0.79, p < 0.001).
On the basis of equal misclassification rates, a cut-off value of
1.80 and 1.36 for rCBV and rCBF ratios, respectively (sensitivity
%100, specifity %84.6 for rCBV and sensitivity %100, specifity %76.9
for rCBF), best discriminated low and high-grade gliomas. Eleven
of thirteen low grade tumors were grade 2 oligodendroglioma and
two of eleven oligodendroglioma showed rCBV value higher than
1.80. None of high grade tumors had rCBV value of lower than 1.80.
(Fig. 4)
4. Discussion
Glial tumors are the most common group amongst primary
brain tumors. Tumoral angiogenesis is one of the most important
factors for assessing grade of gliomas. Tumoral vascularity can be
assessed non-invasively with various perfusion MRI applications.
Conventional MRI sequences are not very sensitive for grading gliomas. Contrast enhancement evaluated with conventional
Please cite this article in press as: Cebeci H, et al. Assesment of perfusion in glial tumors with arterial spin labeling; comparison with
dynamic susceptibility contrast method. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.07.002
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Fig. 2. A 65 years old woman diagnosed with glioblastome multiforme. T1W (A) and postcontast T1W (B) MR images show a large, enhancing mass in the right frontal lobe.
CBV (C) and CBF (D) maps from DSC-PI, ASL subtraction image (E) and CBF map (F) from ASL-PI show hyperperfusion in tumoral lesion.
Fig. 3. Receiver operating characteristic curves for, DSC-rCBV and DSC-rCBF, rCBF-ASL, rSI-ASL and CBF-ASL.
Please cite this article in press as: Cebeci H, et al. Assesment of perfusion in glial tumors with arterial spin labeling; comparison with
dynamic susceptibility contrast method. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.07.002
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Fig. 4. Scatter plot graphs of DSC-rCBV, DSC-rCBF, rCBF-ASL, rSI-ASL and CBF-ASL that representing low and high grade tumors.
sequences means disturbance of blood brain barrier, not exactly
the vascularization [3]. On the other hand, there are quite a few
nonenhancing high-grade tumors. Radiological tumoral grade of
nonenhancing malign gliomas may be assumed as lower, possibly resulting in wrong treatment approaches [10]. In this study,
3 out of thirteen low grade tumors were enhancing and 1 out of
twenty high grade gliomas was nonenhancing. Our results suggest
that enhancement is not a reliable factor for determining tumoral
grade, similarly with previous results.
Previous studies reported that DSC-PI provided useful information about glioma grading [3,10]. More recently, some studies
suggested that ASL is also capable of differentiating low and highgrade gliomas [11,12]. Our findings confirm those of previous
studies showing a strong positive correlation between the degree
of elevated perfusion parameters and tumor grade [13–16].
rCBV calculated out of DSC-PI is commonly used in in evaluating perfusion in brain tumors, but some studies also used rCBF for
grading gliomas [3]. According to our results, both rCBV and rCBF
were significantly different between low and high-grade gliomas.
However, the cutoff value of 1.80 for rCBV had a higher specificity
than the cut of value of 1.36 for rCBF. DSCPI provides both rCBF and
rCBV data, but ASL can only result in an rCBF estimate. Although
there have been some animal experiments to measure CBV with
ASL, there has not been a measurement of CBV with ASL in clinical
practice yet [12].
DSC perfusion imaging is the most commonly used modality for
perfusion assessment in clinical practice. On the other hand, ASL is a
promising technique that does not require contrast agent injection.
According to our results, ASL perfusion parameters, which were
relative signal intensity and relative cerebral flow, could differentiate low and high-grade tumors. Absolute CBF values obtained with
ASL was also capable of differentiating tumoral grade, but we think
relative values were more reliable. To our knowledge, there is no
consensus about the absolute CBF values calculated out of ASL of
low and high-grade gliomas.
Warmuth et al. [10] reported strong positive correlation
between CBF measurements on DSC and ASL perfusion maps.
Pulsed ASL method with a single TI point was used in their study.
But, this may lead to serious errors due to the sensitivity of CBF measurements to arterial transit times [17]. Bolus saturation sequences
such as QUIPSS II were developed to render ASL less sensitive to
transit time, but if the arterial transit time is wide, image acquisition
in multiple TI points and modelling CBF might solve this problem.
Another study that compared DSC and ASL perfusion imaging was
done by Hirai et al. [12] for 24 gliomas at 3T. They also found an
agreement between DSC and ASL.
Noguchi et al. [11] compared percent signal intensity (%SI) and
histopathological microvessel area in 35 brain tumor patients. A
positive correlation was observed between ASL signal intensity and
histopathological microvascular area, and they reported that %SI
on ASL reflected tumoral vascularity in brain tumors. In agreement
with these results, our study showed standardized signal intensity
(rSI) on ASL could differentiate low and high-grade gliomas, and it
was highly correlated with rCBV on DSC perfusion imaging (r = 0.83,
p < 0.001).
Also rSI measurements were highly correlated with rCBF for ASL
data (r = 0.90, p < 0.001).
According to these results, we suggest that measuring signal
intensity on ASL subtraction image may be valuable for grading
gliomas, although, it does not provide a CBF estimate.
Another study that supports this opinion was done by Kimura
et al. [5] for a group of meningioma patients. According to their
results, there was also a strong correlation between %SI and
histopathological data for continuous ASL (r = 0.91, p < 0.001), but
correlation between rCBF and histopathological data was weaker
(r = 0.61, p < 0.001).
Please cite this article in press as: Cebeci H, et al. Assesment of perfusion in glial tumors with arterial spin labeling; comparison with
dynamic susceptibility contrast method. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.07.002
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Lev et al. [18] investigated glial tumor grade and DSC-PI
rCBV treshold and confounding effect of elevated rCBV of oligodendrogliomas. They found rCBV of 1.5 treshold value for best
discrimination low from high grade gliomas, whereas our treshold value for rCBV was 1.80. Our results were consistent with Lev
et al. about confounding effects of oligodendrogliomas. So that two
low grade oligodendrogliomas showed rCBV value of higher than
treshold and also other perfusion parameters of both DSC-PI and
ASL-PI were higher than treshold for these two low grade oligodendroglioma.
No need of intravenous contrast agent injection is the major
advantage of ASL, which makes ASL easy repeatable. ASL may also
be useful in patients with renal failure, because they may be at
risk for contrast-related nephrogenic systemic fibrosis, and in children for whom the intravenous rapid bolus injection of contrast
agents may be difficult [12]. However, over 20 years after development of first ASL sequences, ASL still has not been utilized in
routine clinical practice. Low signal to noise ratio (SNR) is the major
cause of this issue. Therefore, ASL technique needs multiple repetitions for higher SNR, which causes longer imaging times. This
study had some limitations. Contrast enhancement seen in most
of the high-grade tumors may have lead to an underestimation of
rCBV and rCBF values in DSC perfusion imaging. Also, CBF measurement in ASL was hard in some regions due to low SNR. This effect
was especially significant in posterior fossa lesions. Low spatial resolution (3.5 × 3.5 × 6 mm) and limited imaging plane (6 sections,
3.9 cm total width) were other technical limitations of ASL imaging. Although, this study included quite a few patients, there were
no grade 2 astrocytomas in the low-grade group and eleven out
of thirteen lesions were grade 2 oligodendrogliomas. However, all
lesions in this study had histologically proven diagnoses, and all MR
imaging examinations were done at a high magnetic field of 3T. SNR
is higher in high magnetic field thus leading decreased motion artifacts compared to 1.5T. ASL image acquisition at multiple sections
at multiple time points was also an advantage of this study.
Motion artifacts were detected in perfusion MR images especially ASL-PI images because of low temporal resolution. Magnetic
susceptibility artifacts in echo-planar imaging were prominent
at bone-air interfaces and around operation materials. However,
none of the tumors studied was markedly distorted by these
artifacts.
5. Conclusion
Both perfusion MRI techniques, ASL and DSC, were successful
in discriminating low and high grade gliomas. DSC is more commonly used in routine clinical practice and is a widely accepted
method for perfusion imaging in the brain. Despite this fact, ASL
is a promising perfusion imaging method having the advantage of
being non-invasive. According to the results of this study, perfusion
parameters obtained by these two techniques were positively correlated. DSC has the advantage of high SNR and lower imaging time,
and could be preferred in diseases with delayed arterial transit time,
like atherosclerosis. However, a relatively newer non-invasive perfusion method, ASL, may obtain results that are in good agreement
with DSC perfusion imaging, and it may be a useful alternative
method for evaluating the perfusion of glial tumors, especially for
patients with contraindications to contrast agents.
Conflict of interest statement
We confirm that there are no actual and potential conflicts of
interest associated with this publication and there has been no
financial support for this work.
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Please cite this article in press as: Cebeci H, et al. Assesment of perfusion in glial tumors with arterial spin labeling; comparison with
dynamic susceptibility contrast method. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.07.002